Genesis: The Scientific Quest for Life's Origin

by Robert M. Hazen

  p. 91 Other chemists: See Shapiro (1988) for a measured assessment of efforts to synthesize ribose by plausible prebiotic pathways.

  p. 92 Orgel and co-workers: Sanchez et al. (1966). It is important to note that global dilution need not imply local dilution. Regarding this point, Louis Allamandola writes: “This is where I think an exogenic ice/ice residue has a great intrinsic advantage over endogenous processes, even given the total amounts are small with respect to a planetary reservoir. These ices and residues are not dilute.” [Louis Allamandola to RMH, 6 July 2004]

  p. 92 the longest experiments: The use of freezing to synthesize HCN polymers is related in Wills and Bada (2000, pp. 51-52).

  p. 92 by the 1960s: The composition of the Archean Earth's atmosphere is a matter of significant debate. Few scientists today accept Miller's model atmosphere of methane, ammonia, and hydrogen. The majority view is that carbon dioxide and nitrogen were the dominant constituents of a relative unreactive atmosphere (H. D. Holland 1984; Walker 1986; Kasting 1990, 1993, 1994, 2001). Hiroshi Ohmoto of Pennsylvania State University, by contrast, has long argued that the early atmosphere featured significant oxygen content (Ohmoto et al. 1993, Ohmoto 1997). Tian et al. (2005) proposed an alternative hydrogen-rich atmosphere.

  Nevertheless, it is likely that local pockets of reducing gases may have promoted organic synthesis. [Jack Szostak to RMH, 21 August 2004] Bada (2004) writes, “Even though reducing conditions may not have existed on a global scale, localized high concentrations of reduced gases may have existed around volcanic eruptions…. The localized release of reduced gases by volcanic eruptions on the early Earth would likely have been immediately exposed to intense lightning” (p. 6).

  p. 93 Miller and his supporters continue to counter: There is a kind of logic to the argument that the early atmosphere must have been reducing because the resulting synthesis mimics biochemistry. Orgel (1998a, p. 491) states, “It is hard to believe that the ease with which sugars, amino acids, purines and pyrimidines are formed under reducing-atmosphere conditions is either a coincidence or a false clue planted by a malicious creator.”

  p. 93 “If God did not …”: as quoted in Wills and Bada (2000, p. 41).

  p. 93 extremely dilute solution: The improbability of biochemical reactions arising from the dilute primordial soup has emerged as the central objection to the Miller hypothesis in the theories of Günter Wächtershäuser. In a dilute solution with hundreds or thousands of different solutes, the chance that a desired chemical reaction will occur between any two molecules is small. He states, “As far as I'm concerned, the soup theory is more of a myth than a theory, because it doesn't explain anything.” (Hagmann 2002, p. 2007). For a more comprehensive critique, see Wächtershäuser (1994).

  p. 93 another nagging problem: Stanley Miller himself often acknowledges this difficulty. In a 1992 Discover article, he said, “The first step, making the monomers, that's easy. We understand it pretty well. But then you have to make the first self-replicating polymers…. Nobody knows how it's done.” (Radetsky 1992, p. 78). Miller repeated this refrain in a 1998 Discover article: “It's a problem. How do you make polymers? That's not so easy.” (Radetsky 1998, p. 36).

  7

  HEAVEN OR HELL?

  p. 95 “It is we …”: Gold (1999, p. v).

  p. 96 Metabolism: For a useful overview of the surprising diversity of microbial metabolism, see Nealson (1997a).

  p. 96 Our view of life: For a description of this research, see Radetsky (1992).

  p. 97 On this particular dive: In 1979, scientists discovered that some of these vents spew out lots of dissolved minerals that precipitate in a thick black cloud as ocean and vent waters mix—a so-called “black smoker.”

  p. 97 “Could the hydrothermal vents …”: Jack Corliss as quoted in Radetsky (1992, p. 76).

  p. 97 others close to the story: [John Baross to RMH, 24 June 1998 and 10 March 2004; Sarah Hoffman to RMH, 23 July 2004] Jack Corliss did not respond to requests for information. Hoffman provided a 28-page document with a detailed history of the development of the hydrothermal-origins hypothesis and its subsequent presentation at lectures and in print.

  p. 98 “ideal reactors …”: Corliss et al. (1981, p. 62).

  p. 98 much too hot: Several papers from the Miller group focus on the supposed instability of amino acids under hydrothermal conditions, including S. L. Miller and Bada (1988), Bada et al. (1995), and Bada and Lazcano (2002). Other authors attempted to counter these arguments (Holm 1992).

  p. 98 “… a real loser”: Stanley Miller as quoted in Radetsky (1992, p. 82).

  p. 99 Eventually the Corliss: The Corliss et al. (1981) paper appeared in a supplementary section of papers presented at a symposium on the “Geology of the Oceans,” which was part of the 26th International Geological Congress in Paris. A later paper was authored by Baross and Hoffman (1985).

  p. 99 John Baross remains active: Much of John Baross's recent work focuses on barophilic (pressure-loving) and thermophilic (heat-loving) microbes. See, for example, Baross and Deming (1995).

  p. 99 Sarah Hoffman's graduate: Corliss's abandonment of origins research was underscored when he delivered a lecture on his origin hypothesis, “Emergence of Living Systems in Archean Sea Floor Hot Springs,” at the Geophysical Laboratory on January 8, 2001. The lecture offered no new insights beyond his work of the 1980s; indeed, he often interjected that “this is a 1986 lecture.” He seemed to forget many of the details of his model—temperatures, depths, organic chemistry—and his answers to several questions were vague and uninformative.

  p. 100 Everywhere they looked: Dozens of recent books and articles document microbes in extreme environments (Madigan and Marrs 1997, Wharton 2002), including Antarctic ice (Price 2000, Thomas and Dieckmann 2002), boiling hot springs (Stetter et al. 1990, Hoffman 2001), acidic pools and streams (Zettler et al. 2002), deep-ocean hydrothermal zones (Pedersen 1993), and crustal rocks (Krumholz et al. 1997, Chapelle et al. 2002).

  Concurrent with discoveries of abundant deep microbes were the findings of molecular biologist Carl Woese (Woese and Fox 1977; Woese 1978, 1987). Woese applied the techniques of molecular phylogeny to construct a tree of life (see Chapter 10). He discovered that the traditional divisions of life into five kingdoms was incorrect and that the most primitive living cells (i.e., microbes deeply rooted in the evolutionary tree of life) are extremophiles that live in hydrothermal conditions (Pace 1997). This result suggested to some researchers that the first life-forms might have been similar extremophiles. Such a conclusion is not certain, however, because life might have arisen in a cooler surface environment and subsequently radiated into extreme environments. A large impact might then have killed off all surface organisms, leaving extremophiles as our last common ancestors.

  p. 100 Savannah River: Frederickson and Onstott (1996) provide a popular account of this research.

  p. 100 loaded with microbes: The Savannah River samples from a depth of 400 meters support from 100 to 10 million microbes per gram of rock. By comparison, a typical gram of topsoil might hold a billion microbes per gram.

  p. 101 Subsequent drilling studies: Parkes et al. (1993), Stevens and McKinley (1995), Krumholz et al. (1997), Pedersen et al. (1997), Chapelle et al. (2002), and D'Hondt et al. (2002, 2004).

  p. 101 Tullis Onstott: Frederickson et al. (1997), Colwell et al. (1997), Tseng and Onstott (1998) and Onstott et al. (1998). For popular accounts of this research, see Frederickson and Onstott (1996), Monastersky (1997), and Kerr (2002b).

  p. 101 “It was ‘Don't …' ”: Schultz (1999, p. 1).

  p. 102 Thomas Gold: Bondi (2004).

  p. 103 In 1977: Gold (1977). The first peer-reviewed publication of these ideas appeared two years later (Gold 1979). See also Gold and Soter (1980).

  p. 104 Siljan Ring: Gold (1999, pp. 105-123).

  p. 104 Seven years: The controversy was summarized for Science by reporter Richard Kerr (1990). Additional points of view are provided by Donofrio (2003) and by rev
iewers of Gold's book (Brown 1999, Margulis 1999, Parkes 1999, Von Damm 1999). Brown's review in American Scientist, “Upwelling of Hot Gas,” is particularly contemptuous. Few authors seem to have considered the possibility of a middle ground. Might hydrocarbons arise from both surface life and from deep sources? After all, there's a lot of carbon, and hydrocarbons happen.

  p. 104 “the deep hot biosphere”: Gold (1992, 1997, 1999).

  p. 104 invited Gold: The seminar, entitled “The Deep Hot Biosphere,” took place on April 28, 1998.

  p. 105 Tommy Gold helped: Gold died on June 22, 2004, two weeks after suffering a massive heart attack. On June 7, 2004, he had sent me a preliminary review of the first half of this book. “The only comment I want to make before I have read it all very carefully is that you refer too often to the ocean vents,” he wrote. He argued that many other deep environments also contribute organic molecules and might have been more conducive to the origin of life. “But more about all this when I have read with some care what you sent me.” Sadly, that addendum never came. [Thomas Gold to RMH, 7 June 2004]

  p. 105 Heaven Versus Hell: A version of this text appeared in Hazen (1998).

  p. 106 ancient Mars or Venus: Speculations on the habitability of various bodies in the solar system include Reynolds et al. (1983), Sagan et al. (1992), Thompson and Sagan (1992), and Boston et al. (1992).

  8

  UNDER PRESSURE

  p. 107 “Where is this …”: Wächtershäuser (1988a, p. 480).

  p. 108 Geophysical Laboratory: High-pressure research at the Geophysical Laboratory is described in Hazen (1993) and Yoder (2004). For a general history of the Carnegie Institution, see Trefil and Hazen (2002).

  p. 108 well funded by NASA: NASA's Astrobiology Institute (NAI) was founded in 1998 with the Carnegie Institution as one of 11 charter research teams. Additional groups were added in 2001 and 2003. For more information, see the NAI Web site: http://nai.arc.nasa.gov.

  p. 108 Our first experiments: Cody et al. (2000).

  p. 108 In a later set of experiments: Brandes et al. (1998).

  p. 108 Carrying on with this line: Brandes et al. (2000).

  p. 109 “This proposal is based …”: S. L. Miller and Bada (1988, p. 609).

  p. 109 “a real loser”: Stanley Miller as quoted in Radetsky (1992, p. 82).

  p. 110 again and again: These quotes appear in Wills and Bada (2000, pp. 98 and 101). “Ventists,” annoyed at this condescending label, have been known to refer to Bada and colleagues as “Millerites”—or, after a couple of beers, “Miller lites.” In fact, the name “ventists” was coined by RPI chemist James Ferris, who also dubbed Miller and his followers “arcists” (as quoted in Simoneit 1995, p. 133).

  p. 111 roles as varied: The possible roles of minerals in life's origin are reviewed by Hazen (2001).

  p. 111 “Before enzymes …”: Wächtershäuser's ideas initially appeared in four papers (Wächtershäuser 1988a, 1988b, 1990a, 1990b). The central tenets were summarized in “Pyrite formation, the first energy source for life: A hypothesis” (Wächtershäuser 1988b), which emphasizes the role that Popperian philosophy played in the theoretical effort. That paper was submitted to Systematic Applied Microbiology in March of 1988 and published later that year. A more elaborate presentation, “Before enzymes and templates: Theory of surface metabolism” (Wächtershäuser 1988a) soon followed in Microbiology Review. The paper that first brought his ideas to the attention of a wide audience appeared two years later in the Proceedings of the National Academy of Sciences (Wächtershäuser 1990a). Articles submitted to the Proceedings are often communicated by an Academy member; Wächtershäuser's paper, “Evolution of the first metabolic cycles,” was sponsored by Karl Popper himself. The full-blown theory is articulated in the massive “Groundworks for an evolutionary biochemistry: The iron–sulfur world” (Wächtershäuser 1992). Several subsequent papers clarify and elaborate on the model and respond to a growing barrage of comment and criticism (Wächtershäuser 1993, 1994, 1997).

  p. 111 Karl Popper: Popper's key ideas are summarized in three of his books, The Logic of Scientific Discovery (Popper 1959), Conjectures and Refutations: The Growth of Scientific Knowledge (Popper 1963), and Objective Knowledge: An Evolutionary Approach (Popper 1972). Wächtershäuser's presentation of his own hypothesis in terms of “Theory Darwinism” (essentially, competition among rival hypotheses and survival of the fittest) is most clearly presented in Wächtershäuser (1988a).

  p. 111 “During breakfast …”: As quoted in Nicholas Wade, “Gunter Wachtershauser: Amateur Shakes up on Recipe for Life” (New York Times, April 22, 1997).

  p. 112 patched together a theory: A number of widely cited origin-of-life hypotheses, including those based on a primordial soup, can be criticized for their poor predictive ability.

  p. 113 “You don't mind …”: Günter Wächtershäuser as quoted in Radetsky (1998, p. 36). Experiments designed to test aspects of Wächtershäuser's theory include Blöchl et al. (1992), Keller et al. (1994), Huber and Wächtershäuser (1997, 1998), and Huber et al. (2003).

  p. 113 “It takes maybe two weeks”: Günter Wächtershäuser in response to Robert Hazen at his Geophysical Laboratory seminar, March 23, 1998. Other estimates vary widely. De Duve (1995b, p. 428) suggests, “millennia or centuries, perhaps even less.” See also Lazcano and Miller (1994) and Fry (2000, pp. 125-126).

  p. 113 “not a new idea”: Bada and Lazcano (2002, p. 1983). The paper they refer to, “A note on the origin of life” (Ycas 1955), introduces the idea of an autocatalytic cycle of metabolites as the first living system. Dick and Strick (2004, p. 64) agree that “Ycas had pioneered the ‘metabolism first' idea.” However, Noam Lahav notes that Alexander's (1948) discussion of autocatalysis predates that of Ycas. [Noam Lahav to RMH, 27 August 2004]

  p. 114 January 1998: “We have not met, but your work of the past decade on the role of sulfides in organic synthesis and the origin of life is having a profound effect on our current research,” I wrote. “We would be delighted if you could schedule a trip to the States, for which we would pay expenses.” [RMH to Günter Wächtershäuser, 14 January 1998]

  p. 114 Wächtershäuser delivered his lecture: The Geophysical Laboratory seminar, “Chemoautotrophic Origin of Life in an Iron–Nickel–Sulfur World,” took place on March 23, 1998.

  p. 114 “We would like to explore …”: [RMH to Günter Wächtershäuser, 8 April 1998]

  p. 115 I was left: That memorable meeting was the last contact any of us had with Günter Wächtershäuser until Harold Morowitz received a stern letter on Wächtershäuser & Hartz legal stationary dated October 11, 2000. Copies of the letter were also sent to the bosses of everyone involved, including Bruce Alberts, president of the National Academy of Sciences; Maxine Singer, president of the Carnegie Institution; and Alan Merten, president of George Mason University. Harold Morowitz, with three coauthors (including George Cody), had recently published a short article in the Proceedings of the National Academy of Sciences on life's most primitive metabolic cycle. Morowitz et al. (2000) proposed that molecules used in the so-called “reductive citric acid cycle” (what I refer to in the text as the “reverse citric acid cycle”) are highly selected, with a long list of distinctive features. Such selectivity, Harold concluded, suggests that life's earliest metabolism is deterministic and likely to be the same on any planet or moon where life emerges. Wächtershäuser denounced the article as improperly claiming credit for ideas that were originally his, and he demanded an immediate retraction. Harold ignored the veiled threat of legal action, but we were saddened that a brilliant man with such creativity and vision could so remove himself from the cooperative spirit of scientific research.

  p. 115 His first paper: Brandes et al. (1998).

  p. 115 He followed up: Brandes et al. (2000).

  p. 115 In spite of these successes: Bada et al. (1995). The hydrothermal stability of amino acids is also discussed by Shock (1990b), Hennet et al. (1992), and W. L. Marshall (1994).

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p; p. 116 a few centuries: Wolfenden and Snider (2001).

  p. 116 preserve proteins: Recent studies on the essential bone protein osteocalcin underscores the ability of minerals to stabilize organic molecules. Hoang et al. (2003) document the complex structure of osteocalcin and illustrate how it binds strongly to hydroxyapatite, the principal mineral constituent of bone. This binding not only provides strength and flexibility to bone but also protects osteocalcin from the rapid decay experienced by most other proteins. Christine Nielsen-Marsh and co-workers at the University of Newcastle (Nielsen-Marsh et al. 2002) exploit this feature to extract and sequence osteocalcin from fossil bison bones more than 50,000 years old. Over time, osteocalcin undergoes slight mutations in its amino acid sequence. Comparison of small differences in this sequence among fossils of various species and ages thus reveals patterns of mammalian evolution.

  Bruce Runnegar writes, “I'm skeptical of the report of collagen in dinosaur bone. Osteocalcin maybe, but I wait to be convinced about collagen.” [B. Runnegar to RMH, 4 March 2005]

  p. 116 Additional evidence: Lemke et al. (2002) and Ross et al. (2002a, 2002b).

  p. 117 molecules might separate out: The idea of the separation from water of an amino-acid-rich phase first appeared in von Nägeli (1884). This idea was also a central feature of Oparin's original hypothesis (Oparin 1924, 1938), as well as several subsequent proposals. See, for example, Fox and Harada (1958) and Fox (1965, 1988).

  p. 117 more work to be done: In spite of these results, David Ross emphasizes that amino acids cannot survive long enough in a hydrothermal environment to start life. “The utility of hydrothermal work is that it allows us to accelerate reactions to convenient times so that we can study them. No more than that…. The key reactions leading to life involved very, very slow reactions. Half-lives of a million years or more would be the order of the day, and it would take a graduate student of unusual longevity, durability, and endurance to get any data on such reactions.” [David Ross to RMH, 14 July 2004]